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Evolution of the Y-Chromosome in Primates Audrey Marsh Western Washington University, [email protected]

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Evolution of the Y-Chromosome in Primates Audrey Marsh Western Washington University, Ajmarsh7@Gmail.Com Western Washington University Western CEDAR Western Libraries Undergraduate Research Award Western Libraries and the Learning Commons 2014 Evolution of the Y-Chromosome in Primates Audrey Marsh Western Washington University, [email protected] Follow this and additional works at: https://cedar.wwu.edu/library_researchaward Part of the Biology Commons Recommended Citation Marsh, Audrey, "Evolution of the Y-Chromosome in Primates" (2014). Western Libraries Undergraduate Research Award. 1. https://cedar.wwu.edu/library_researchaward/1 This Research Paper is brought to you for free and open access by the Western Libraries and the Learning Commons at Western CEDAR. It has been accepted for inclusion in Western Libraries Undergraduate Research Award by an authorized administrator of Western CEDAR. For more information, please contact [email protected]. Marsh 1 Audrey Marsh W01010313 Bio 432 3/17/14 Evolution of the Y-chromosome in Primates The primate X and Y chromosomes are believed to have diverged from a set of ancestral autosomes that over time accumulated enough genetic differences to make them mostly non- homologous. More specifically, since its appearance approximately 166 million years ago the Y- chromosomes has been plagued by a series of mutational deletions that has shortened its length dramatically (Warren et al., 2008). The evolution of the Y-chromosome and its degradation therefore has radically changed the active genes that were once present in common ancestors from those living today (Charlesworth, 2000). However, its massive erosion over time has become somewhat of a concern, as it leads to questions of whether or not the Y-chromosome is on the path to extinction. To answer this question, a detailed analysis on the historical divergence of the Y- chromosome, as well as an investigation on the evolutionary mechanisms molding the Y- chromosome is needed to determine whether or not the male sex is on the brink of extinction. The Structure of the Primate Y-chromosome A brief overview of the makeup of the Y-chromosome in primates will give insight into why it shrinks so readily. Today, the human Y-chromosome contains approximately 50,000 base pairs that have been mapped to correlate 86 functional genes on the Y-chromosome (Payer et al. 2008). Geneticists have partitioned the Y-chromosome into two main regions (Figure 1): the pseudoautosomal region (PAR), and the male specific region (MYS). The PAR is the terminal homologous regions (chimps and macaques only have one PAR; humans have two) that are Marsh 2 capable of undergoing meiotic recombination with its paired X-chromosome, making it the only region on the Y-chromosome that is capable of any recombination (Rappold, 1993). The remainder of the chromosome is defined as the MYS region, which codes for all the male sex differentiating material that distinguishes itself from the X-chromosome (Hughes et. al 2012). Scientist have further broken down the MYS region into five more distinct zones. The heterochromatic portion of the Y-chromosome is the area in which DNA is tightly packed together to give greater control over gene expression. Researchers currently have the least amount of data on these sections, however they seem to vary in length across primate species. Next, the X-transposed region refers to the area of the Y-chromosome which is believed to have been transferred from an ancestral X- chromosome somewhere around three to four million years ago. Similarly, the X-degenerate region on the Y-chromosome shows a relation to an ancestral X-chromosome, except in that it was not transposed, but rather is an ancestral remnant of the autosome that the X and Y chromosome came from sometime before its diversification. As its name would suggest, this region of the Y- chromosome has severely deteriorated over time since its divergence (Bachtrog 2013). Finally, and maybe most importantly, there are several ampliconic regions of the Y-chromosome. These regions are characterized by repetitive palindromic sequences of DNA that house different highly copied genes that express traits for male gonad differentiation in development. Important genes that are found in this region include the SYR gene (aids in testes development), and the DAZ gene (promotes healthy spermagenesis) (Yueh-Hsiang et al. 2008). The length of these ampliconic regions vary greatly by primates species, as chimpanzees and humans have the longest regions being 14.7Mb and 10.2Mb respectively, while macaques have a significantly shorter sequence that is only about .5Mb (Bachtrog 2013). As stated earlier the MYS cannot undergo recombination with the X-chromosome. This allows mutations to accumulate in the MYS during DNA replication Marsh 3 that will, consequently, be identically passed down father to son because its lack of recombination prevents variation on this region. Therefore, without variation natural selection cannot act upon the chromosome because there is no force that can remove the deleterious mutations out of the population. This highlights the importance of the ampliconic region as it acts as a homologous region for itself and therefore can protect important genes (most vital sex determining genes are in the ampliconic region) by recombining with itself just as regular autosomal recombination would do. This also essentially allows the chromosomes to undergo purifying selection by itself, and remove large portions of DNA that may have accumulated deleterious mutations (Griffen, 2012). Hence, the repetitive nature of this region makes the Y-chromosome easily susceptible to mutational deletion, and is most likely the source of why it is so dynamic in length over time (Hughes et al., 2012). Phylogenetic Analysis of Y-chromosome Evolution The origin of the Y-chromosome predates the primate order, and is believed to have emerged somewhere early in the evolutionary history of mammals. Its genesis was caused by a major mutation that rearranged the proto Y-chromosome significantly enough that it could no longer recombine with its autosomal twin. It is suggested, however, that the Y-chromosome did not bear its sex determining function till the addition of genes like SRY that aid in testicle development (Graves, 1995). The disrupt in homology between the proto-X and proto-Y allowed for selection to act on the Y to promote further differentiate from the X-chromosome through time (Bachtrog, 2006). The emergence of the mammalian Y-chromosome was a homoplasious event, as sex chromosomes are observed across many different classes (Graves, 2001). Evidence for homoplasy was determined through a comparison of the mammalian Y-chromosome with the sex determining Marsh 4 genes of birds and reptiles. In contrast to mammals, birds and reptiles have sex chromosomes dubbed ZZ and ZW, where birds in particular have heterogametic females and homogametic males (Raymond et al., 1999). Furthermore, a comparison of the SRY gene on the mammalian Y- chromosome with the analogous DMRT1 gene on the avian/reptilian Y shows no evolutionary relationship between the two. These findings led to the conclusion that the mammalian Y- chromosome had to independently appear sometime in the very early existence of the mammals, and most likely appeared in its most basal group the monotremes (Figure 2) (Veyrunes et al., 2008). A closer investigation of the monotreme’s sex chromosomes reveals a complicated evolutionary pathway of the XY chromosome structure of therian mammals. The platypus, a modern day monotreme, has five pairs of sex chromosomes that align in a chain like structure in which XX denotes a female and XY male (Grützner, 2006). A comparison of these X- chromosomes with other vertebrate sex chromosomes reveals that they share several regions of homology with avian sex chromosomes, but none with the therian sex chromosomes. Hence, further supporting the hypotheses that the therian Y-chromosome most likely diverged convergently from avian/monotreme sex chromosomes. Further comparisons of the platypus genome with therian sex chromosomes revealed an ancestral relationship between the autosomal chromosome 6 on the platypus indicating this may have been the autosome in which the therian Y and X chromosomes diverged from (Veyrunes et al. 2008). The divergence of autosome 6 into the Y-chromosome is hypothesized to occur through a transposition in which the autosome acquired the x-linked SOX3 gene which is expressed in both avian male and female sexual organs. Homology between the SOX3 and SYR gene indicate that the SOX3 might be a distant relative of the SYR (Figure 3). It is therefore most likely that this mutation triggered selection to act on the SOX3 gene to become a more male defining trait in which over time has further specialized it to Marsh 5 relate to sex determination (Graves, 2008). These findings effectively date the mammalian Y- chromosome to independently appear no earlier than 166 million years ago with the appearance of monotremes, and no later than 148 million year ago with the appearance of therians (Veyrunes et al. 2008). Looking more specifically into the Y-chromosome of the primate order, it becomes apparent that it has endured a series of mutations that vary the Y-chromosome across primate species. The azoospermia factor (AZFc) is a multi-ampliconic region on the Y-chromosome that houses many of the important male-defining genes found in higher primate lineages; deletions or complex mutations within this area often result in infertility in males (Kuroda-Kawaguchi, 2001). Most of the amplicons found in the AZFc were transposed from ancestral autosomes into the Y- chromosome at various points in time during primate evolution. The major transposition events of the AZFc in primates is hypothesized to have occurred in three different waves. The first wave occurred just after the divergence of the new world monkeys approximately 35 million years ago, in which two major ampliconic regions, denoted green and red in the literature (Figure 4), were inserted into the primate Y-chromosome and subsequently duplicated into high copy numbers.
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